Skip to main content

Main menu

  • HOME
  • CONTENT
    • Early Release
    • Featured
    • Current Issue
    • Issue Archive
    • Collections
    • Podcast
  • ALERTS
  • FOR AUTHORS
    • Information for Authors
    • Fees
    • Journal Clubs
    • eLetters
    • Submit
  • EDITORIAL BOARD
  • ABOUT
    • Overview
    • Advertise
    • For the Media
    • Rights and Permissions
    • Privacy Policy
    • Feedback
  • SUBSCRIBE

User menu

  • Log out
  • Log in
  • My Cart

Search

  • Advanced search
Journal of Neuroscience
  • Log out
  • Log in
  • My Cart
Journal of Neuroscience

Advanced Search

Submit a Manuscript
  • HOME
  • CONTENT
    • Early Release
    • Featured
    • Current Issue
    • Issue Archive
    • Collections
    • Podcast
  • ALERTS
  • FOR AUTHORS
    • Information for Authors
    • Fees
    • Journal Clubs
    • eLetters
    • Submit
  • EDITORIAL BOARD
  • ABOUT
    • Overview
    • Advertise
    • For the Media
    • Rights and Permissions
    • Privacy Policy
    • Feedback
  • SUBSCRIBE
PreviousNext
Articles, Development/Plasticity/Repair

Modeling Transformations of Neurodevelopmental Sequences across Mammalian Species

Alan D. Workman, Christine J. Charvet, Barbara Clancy, Richard B. Darlington and Barbara L. Finlay
Journal of Neuroscience 24 April 2013, 33 (17) 7368-7383; DOI: https://doi.org/10.1523/JNEUROSCI.5746-12.2013
Alan D. Workman
1Behavioral and Evolutionary Neuroscience Group, Cornell University, Ithaca, New York 14853 and
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Christine J. Charvet
1Behavioral and Evolutionary Neuroscience Group, Cornell University, Ithaca, New York 14853 and
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Barbara Clancy
2Department of Biology, University of Central Arkansas, Conway, Arkansas 72035
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Richard B. Darlington
1Behavioral and Evolutionary Neuroscience Group, Cornell University, Ithaca, New York 14853 and
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Barbara L. Finlay
1Behavioral and Evolutionary Neuroscience Group, Cornell University, Ithaca, New York 14853 and
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • Article
  • Figures & Data
  • Info & Metrics
  • eLetters
  • PDF
Loading

Article Figures & Data

Figures

  • Tables
  • Figure 1.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Figure 1.

    The distribution of the neural location (left) and general class of developmental process (right) of events used to develop the model, plotted against the event scale. The event scale, which is described in more detail in Figure 3, is a ranking of all these events on a scale from 0 to 1, and principally represents their order of occurrence across all of the species. New events added in this data analysis compared with the original model (Clancy et al., 2001) are in red and show not only the addition of late behavioral, physiological, and overall growth information to the model but also addition to the database throughout; events common to both in black.

  • Figure 2.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Figure 2.

    Predicted developmental schedules for human (blue circle), macaque (red circle), cat (yellow circle), short-tailed opossum (green circle), and mouse (black circle), selected from the 18 species to illustrate the full range of developmental durations. In this graph the event scale is the x-axis, to which we have added a subset of the 271 events that were observed. This scale ranges from 0 to 1, but in this case, event scale numerical values are replaced by these example events. As will be described in Figure 3, the event scale is a common ordering of developmental events across all species. The y-axis is the estimated date of occurrence of each event in each species from conception (log scale). To determine when a particular event would be predicted to occur in any species from this graph, using the name of the event on the event scale, find where it intersects the regression line for that particular species. The y-axis value will be the predicted PC day for that event/species combination. In future graphical representations of the event scale, the event scale value for any named event can be found in Table 1. Also represented on this graph are interaction terms for corticogenesis and retinogenesis, with interaction terms always associated with individual species. The parallel lines for a subset of events in four of the species (black bordered circles for human, macaque, cat, and possum) represent delays in cortical neurogenesis with respect to their time of occurrence in the rodent and rabbit. In the cat, a second parallel line can be seen representing the delay of retinal neurogenesis (yellow circle with a black dot).

  • Figure 3.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Figure 3.

    The relation of the event scale used in this analysis to the ordering of events that was used in the prior model. Plotted on the x-axis are the event scores determined by GLM as in Clancy et al. (2001), estimating values for all species-event combinations by determining their overall ranking, and fitting those scores on a scale from 0 to 1.5. The event scale of the present analysis plotted on the y-axis was derived by the quasi-Newton optimization method described in the text. The two values derived for each event are very highly correlated, and also conform to the necessary biological ordering of events (e.g., cell birth before cell death). Each of these two scales was designed to correlate perfectly, within its own dataset, with the estimated Y values for any rodent and rabbit species. This shows that the quasi-Newton optimization method essentially ranks the order of occurrence of events in development, but it differs in two important respects. First, it shows a statistically significant nonlinearity, most obvious in the higher values on each scale. Second, some events fall noticeably above the main regression line, the largest cluster are those to the left of the arrow on the figure, and may represent events in early axonogenesis and GABA-neuron generation, which are either very substantially shifted in their order between species or nonhomologous events.

  • Figure 4.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Figure 4.

    Fit of empirical data to model values in four representative species. The x-axis is the predicted date of occurrence of all the events for which there were also empirical data points; the y-axis is the empirical value of the measured event in that species. As described in several technical aspects in the texts, the fit of predicted to actual days is very high.

  • Figure 5.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Figure 5.

    Plotted are all of the empirically measured developmental events (y-axis) in the cat, versus predicted developmental time for each event (x-axis), before the fitting of a retinal neurogenesis interaction term. All of the events in retinal neurogenesis are highlighted by black circles and all other events are in gray. The retinal neurogenesis events all occur later than would be predicted by the general model for the cat. Consistent with the hypothesis that this developmental delay has occurred for the purpose of increasing the retinal cell populations associated with nocturnality, within the retinal neurogenesis group only retinal ganglion cells are delayed. Retinal ganglion cells are the only measured cell class in the cat retina that are neither rods nor have a connection with rods.

  • Figure 6.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Figure 6.

    Phylogenetic tree plotting the positions of relative delay in cortical neurogenesis, to determine whether delay in onset of cortical neurogenesis, associated with a taxonomic grade shift up in neocortical volume, had occurred at single or multiple times in mammalian phylogeny. Bold pluses and minuses mark branches with delays described in this dataset, and which also have species with increased adult cortical volume, while the unmarked ones represent branches where only relative cortical volume differences in adults are known (Reep et al., 2007). Increases in relative cortical volume appear to have occurred at least three times in mammals, in Metatheria (various marsupials), in the branch giving rise to carnivores, various ungulates, and dolphins, and in primates. It cannot be determined from these data as yet whether a large cortex is the “basal” state, and reduced cortical volume has been selected for in glires, bats, shrews, and Afrotheria, or the reverse. Phylogeny from Song et al. (2012).

  • Figure 7.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Figure 7.

    The maximum duration of neurogenesis across species, plotted on the basic segmental divisions of the embryonic vertebrate nervous system. Only one side of the neural plate is plotted, with the midline to the right, and more alar or lateral locations to the left. Rhombomeres 1–11, which give rise to the medulla, pons, and cerebellum, and the prosomeres, which give rise to the diencephalon and telencephalon, are indicated. The neural plate representation compresses the segmental divisions described previously (Garcia-Lopez et al. (2009) into four medial to lateral divisions. The latest date of neurogenesis observed in each division is plotted on the z-axis, as given by the mean of the species' event scores found there. Extended duration of neurogenesis is more likely in more alar (lateral) and more rostral divisions.

  • Figure 8.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Figure 8.

    Comparison of the modeled relative rates of brain development for a metatherian (marsupial) and a eutherian (placental) mammal of similar adult brain sizes. The marsupial species is the Polyprodonta dunnart, the marsupial mouse, and the placental mammal is a rodent, the common mouse M. musculus. The x-axis is the event scale, and the y-axis shows the predicted PC day of the occurrence of each event in both species. In this graph, the y-axis is a linear, not a log scale, so that the differences in duration can be better appreciated in this case where brain sizes are comparable. The elevated points near the dunnart line represent the effect of the non-glires interaction term delaying cortical neurogenesis with respect to the mouse. The dunnart takes nearly twice as long to reach 80% of its adult brain size compared with the laboratory mouse, with later developmental events disproportionately protracted compared with early events.

  • Figure 9.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Figure 9.

    The position of birth for six placental mammals relative to the event scale (x-axis); the age of each mammal in PC days can be read for birth (or any event scale value) on the y-axis. The five placental mammals are chosen to represent close to the full range of the dataset and include one highly precocial mammal, the guinea pig. For an example, in the mouse at birth cortical neurogenesis is still underway and synaptogenesis in the forebrain is only beginning, while in the guinea pig at birth, cortical neurogenesis, cortical cell migration, and basic axonogenesis is entirely complete, and the point of peak synaptic density has passed (human (blue dot), macaque (red dot), cat (yellow cat), guinea pig (green dot), and mouse (black dot).

  • Figure 10.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Figure 10.

    The relationship of adult brain weight (x-axis, log scale), modeled slope (left), and intercept (right) values for all eutherian mammals. The slope of the modeled regression line (left) can be used as a measure of the number of days, and thus the total developmental duration required to reach the last maturational point measured is closely related to brain weight. The intercept (right), which gives the PC age when the first neurodevelopmental events occur, distinguishes precocial from altricial animals, and also relates to brain size. Of the rodents, for example, the precocial spiny mouse and guinea pig have the highest intercepts, while the altricial mouse and hamster have the lowest.

  • Figure 11.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Figure 11.

    Top, Modeled regression slopes for two highly precocial rodents, the spiny mouse and guinea pig, compared with the altricial mouse (M. musculus) whose brain weight is similar to the spiny mouse, and the relatively altricial ferret, whose brain weight is close to the guinea pig; the regression slope for the macaque is also plotted. x-axis is the event scale, and the y-axis is predicted PC day (logged). Both precocial cases show the delayed onset of in utero neurodevelopment and very rapid progress through developmental stages characteristic of the precocial group. Elevated points associated with the ferret and macaque regression lines are the non-glires*corticogenesis interaction term. Bottom, Empirical data density and distribution, and fit of data to model, for the three most precocial species, the spiny mouse, guinea pig, and sheep. All modeled points are represented in gray, while the points for which there are empirical measurements are black circles.

Tables

  • Figures
    • View popup
    Table 1.

    List of all events with corresponding event scores, sorted by location classification

    LocationEvent scoreLocationEvent scoreLocationEvent score
    Brain stemLimbic system (continued)Cortex (continued)
    Cranial motor nuclei–peak0.038Presubiculum–peak0.261Neurogenesis cortical layer II/III–peak (VC)0.395
    Oculomotor nucleus cell generation–onset0.041Dentate gyrus–peak0.264Cortical axons reach dorsal lateral geniculate nucleus0.396
    Trigeminal mesencephalon nucleus–onset0.041Anterior commissure appears0.267Primary auditory cortex neurogenesis–offset0.420
    Trigeminal mesencephalon nucleus–offset0.041Ventromedial hypothalamus neurogenesis offset0.269Corticospinal tract decussates at the pyramids0.428
    Mesencephalic trigeminal cell generation–offset0.042Mitral cells–offset0.274Corticospinal tract reaches cervical spinal cord0.439
    Trigeminal motor nucleus–peak0.051Suprachiasmatic nucleus neurogenesis offset0.283Initial differentiation of layer V (S1)0.444
    Medial longitudinal fasciculus appears0.062CA1, CA2–peak0.285Cortical axons innervate dorsal lateral geniculate nucleus0.465
    Postproliferative zone in the medulla appears0.073Nucleus accumbens—peak0.294Neurogenesis cortical layer II/III–end (VC)0.490
    Trigeminal motor nucleus–offset0.078Tufted cells–peak0.327Range of rapid synaptogenesis (VC)–start0.501
    Superior colliculus generation–onset0.079Hippocampal commissure appears0.337Onset of barrels (S1)0.504
    Superficial superior colliculus laminae–start0.095Septal nuclei–offset0.339Corticospinal tract reaches dorsal horn of cervical spinal cord0.514
    Postproliferative zone appears in the tegmentum0.112Olfactory tubercle generation–offset0.362Onset of decrease in fractional anisotropy0.515
    Posterior commissure appears0.112Entorhinal cortex neurogenesis offset0.375Onset of sublayers in layer V (S1)0.517
    Lateral cuneate nucleus–onset0.119Hippocampal CA3 neurogenesis offset0.380Onset of trilaminar plate (S1)0.517
    Lateral and medial superior olivary nucleus–onset0.119Hippocampal CA1 neurogenesis offset0.387Adult-like cortical innervation of dorsal lateral geniculate nucleus0.531
    Cranial sensory nuclei–peak0.120Subicular cortex neurogenesis offset0.389Onset of barrel field septa (S1)0.555
    Postproliferative zone appears in the pretectum0.125Granule cells in the dentate gyrus–peak0.583Visual cortical axons in SC0.570
    Medial cuneate nucleus–peak0.135Olfactory tract myelination onset0.634Corticospinal projections reach lumbar levels0.583
    Reticular nuclei—peak0.155Stria medullaris myelination onset0.653First cortical visually evoked potentials0.590
    Postproliferative zone appears in the superior colliculus0.157Fornix myelination onset0.675Corticospinal tract reaches the sacral region0.623
    Inferior colliculus generation–onset0.171Anterior commissure myelination onset0.677Middle cerebellar peduncle myelination onset0.652
    Lateral cuneate nucleus–peak0.186Mammillothalamic tract myelination onset0.689External capsule myelination onset0.666
    Substantia nigra–peak0.187Hippocampus myelination onset0.699Cingulum myelination onset0.687
    Sensory nucleus of the trigeminal nerve–offset0.199Fasciculus retroflexus myelination onset0.700Internal capsule myelination onset0.692
    Lateral and medial superior olivary nucleus–offset0.199Stria terminalis myelination onset0.703Corpus callosum body myelination onset0.722
    Superior colliculus–peak0.202Splenium myelination onset0.732
    Inferior colliculus–peak0.203ThalamusPlasticity/OD critical period–start0.770
    Raphe nucleus neurogenesis–offset0.206Medial geniculate nucleus onset0.113Range of rapid synaptogenesis (VC)–end0.849
    Medial cuneate nucleus–offset0.249Dorsal lateral geniculate nucleus–start0.127Visual cortex peak synaptic density (area 17)0.869
    Pontine nuclei–peak0.255Postproliferative zone appears in thalamus0.144Prefrontal cortex peak synaptic density0.886
    Lateral cuneate nucleus–offset0.262Medial geniculate nucleus–peak0.176Plasticity/OD critical period–end0.901
    Superficial superior colliculus laminae–offset0.279Ventral lateral geniculate nucleus–peak0.177Corpus callosum body myelination end0.971
    Superior colliculus generation–offset0.308Dorsal lateral geniculate nucleus–peak0.183Middle cerebellar peduncle myelination end1.000
    Dopaminergic axons from midbrain reach subplate0.352Ventroposterior and ventrobasal nuclei - peak0.191
    Inferior colliculus generation–offset0.381Ventrobasal neurogenesis - onset0.194Whole brain
    Dopaminergic axons from midbrain reach cortical plate0.395Medial geniculate nucleus offset0.21120% maximum brain weight (day)0.586
    Dopaminergic axons from midbrain in cerebral cortex0.499Dorsal lateral geniculate nucleus–end0.22830% maximum brain weight (day)0.635
    Superficial superior colliculus–start of lamination0.504Anteroventral, anteromedial, anterodorsal nuclei–peak0.23840% maximum brain weight (day)0.682
    Inferior cerebellar peduncle myelination onset0.543Lateral geniculate nucleus axons in subplate0.30550% maximum brain weight (day)0.729
    Superior colliculus segregation0.548ventrobasal neurogenesis–offset0.34160% maximum brain weight (day)0.788
    Ipsi/contra segregation in superior colliculus0.561Pulvinar projections in interior zone of prestriate isocortex0.37570% maximum brain weight (day)0.858
    Medial lemniscus myelination onset0.564Pulvinar projections in subplate of prestriate isocortex0.47180% maximum brain weight (day)0.949
    Posterior commissure myelination onset0.591Pulvinar projections in cortical plate of prestriate isocortex0.515
    Onset of synapse elimination in neurons of the soleus0.629Lateral geniculate nucleus axons in cortical layer IV0.545Whole organism
    Brachium inferior colliculus myelination onset0.664Ipsi/contra segregation in lateral geniculate nucleus0.561Surface righting onset0.573
    Optic radiation myelination onset0.652Rooting reflex offset0.623
    CerebellumAuditory radiation myelination onset0.668Auditory startle reaction0.648
    Inferior olive generation–onset0.058Lateral geniculate nucleus myelination onset0.680Preyer reflex0.681
    Inferior olivary nucleus–peak0.092Vibrissa placing adult like pattern0.695
    Purkinje cell generation–onset0.110Air righting reflex0.730
    Cerebellum (continued)StriatumWhole organism (continued)
    Postproliferative zone appears in the cerebellum0.125Ganglionic eminence postproliferative zone appears0.088Semi-adult-like sleep cycle0.745
    Inferior olive generation–offset0.137Caudatoputamen generation–onset0.131Visual placing is mature0.768
    Purkinje cells–peak0.142Globus pallidus–peak0.140Postconception walking onset0.794
    Deep cerebellar nuclei–peak0.151Claustrum–peak0.147
    Anteroventral cochlear nucleus–peak0.179Caudatoputamen–peak0.186Sensory periphery
    Purkinje cell generation offset0.200Claustrum offset0.308Trigeminal ganglion cell generation–onset0.000
    Cochlear nuclei–peak0.220Caudatoputamen–offset0.519Trigeminal ganglion cell generation–offset0.195
    Superior cerebellar peduncle myelination onset0.564Lateral lemniscus myelination onset0.572Ears open0.668
    Lenticular fasciculus myelination onset0.602
    Limbic systemStriatum myelination onset0.715Retina
    Locus ceruleus–onset0.041Photoreceptor generation–onset0.054
    Locus ceruleus–peak0.059CortexHorizontal cell generation–onset0.059
    Magnocellular basal forebrain–peak0.071Subplate—peak0.071Retinal ganglion cell generation–start0.091
    Mitral cells onset0.085Subplate–onset of neurogenesis0.072Retinal horizontal cells–peak0.153
    Olfactory tubercle generation–onset0.093Neurogenesis cortical layer VI–start (VC)0.117Amacrine generation onset0.158
    White matter appears in the hypothalamus0.097Cortical plate first observed/visible0.123axons in optic stalk0.163
    Preoptic nucleus generation–onset0.102Primary auditory cortex neurogenesis–onset0.136Retinal ganglion cells–peak0.195
    Septal nuclei–onset0.110Cortical subventricular zone–onset0.164Optic axons at chiasm of optic tract0.198
    Locus ceruleus–offset0.113Primary somatosensory cortex–layer VI offset0.194Rapid axon generation in optic nerve–start0.217
    Entorhinal cortex neurogenesis onset0.119Neurogenesis cortical layer V–start (VC)0.203Cones–peak0.264
    Raphe complex–peak0.120Neurogenesis cortical layer VI–peak (VC)0.204Optic axons invade visual centers0.270
    Medial forebrain bundle appears0.125Neocortical layer I emerges0.207Rod generation–onset0.282
    Hippocampal CA3 neurogenesis onset0.139GABA cells in subplate–start0.213Muller cell generation–onset0.282
    Subicular cortex neurogenesis onset0.139External capsule appears0.215Retinal amacrine cells–peak0.298
    Granule cell layer fascia dentata neurogenesis onset0.140Primary somatosensory cortex–layer V offset0.220Bipolar cell generation–start0.300
    Hippocampal CA1 neurogenesis onset0.143Internal capsule appears0.236Optic axons reach dorsal lateral geniculate nucleus and superior colliculus0.319
    Granule cells in the dentate gyrus–onset0.150Lhx6 first in cortex in GABAergic cells0.238Retinal ganglion cell generation–end0.333
    Postproliferative zone appears in the medial pallium0.151GABA cells in subplate–end0.249Horizontal cell generation–offset0.371
    Mammillothalamic tract appears0.153Primary somatosensory cortex–layer 2/3 onset0.255Optic nerve axon number–peak0.392
    Preoptic nucleus–peak0.157Neurogenesis cortical lamina VI–end (VC)0.258Onset of retinal waves stage II0.401
    Fasciculus retroflexus appears0.162Neurogenesis cortical lamina IV–start (VC)0.267Onset of retinal waves stage I0.425
    Stria medullaris thalami appears0.166Neurogenesis cortical layer V–peak (VC)0.268Rods–peak0.464
    Supraoptic nucleus of hypothalamus offset0.169Primary somatosensory cortex–layer IV offset0.283Retinal bipolar cells—peak0.478
    Suprachiasmatic nucleus–peak0.170GABA-ir cells in lower intermediate zone0.286End of retinal waves stage I0.520
    Amygdala–peak0.177GABA positive cells appear in lower intermediate zone0.287Bipolar cells generation–offset0.541
    Mitral cells–peak0.182Peak subventricular zone expansion in the developing isocortex0.289Amacrine cell generation–offset0.552
    Endopiriform neurogenesis offset0.193Subplate and intermediate zone apoptosis onset0.302Rod generation—offset0.561
    Anterior olfactory nucleus–peak0.194Neurogenesis cortical layer V–end (VC)0.305Onset of retinal waves stage III0.573
    Nucleus of lateral olfactory tract–peak0.198Neurogenesis cortical layer IV–peak (VC)0.320Retinal waves0.575
    Septal nuclei–peak0.215Cortical plate apoptosis onset0.321End of retinal waves stage II0.578
    Entorhinal cortex–peak0.230Neurogenesis cortical layer II/III–start (VC)0.342Rapid axon loss in optic nerve ends0.583
    Olfactory tubercle generation–peak0.238Corpus callosum appears0.359Muller cell generation–offset0.597
    Fornix appears0.241Neurogenesis cortical layer IV–end (VC)0.362Optic tract myelination onset0.597
    Stria terminalis appears0.243Layer IV genesis–start0.366Eye opening0.663
    Subiculum–peak0.248Primary somatosensory cortex–layer 2/3 offset0.368First electroretinogram0.665
    Parasubiculum–peak0.252Cortical axons reach thalamus0.371End of retinal waves stage III0.672
    Optic tract myelination end0.847
    • Within location subcategories, events are listed from lowest to highest event score.

    • View popup
    Table 2.

    List of species used in our analysis, sorted by species slope

    SpeciesConstantSlopePrecocial scoreAdult brain weight (g)Adult male body weight (g)Gestational length (days)
    Spiny mouse2.820.6221.3560.74239
    Guinea pig2.9041.5730.841464068.5
    Hamster2.1891.6440.3361.1210815.5
    Rat2.311.7050.445220721
    Gerbil2.5321.7150.4011.027025
    Mouse2.1451.8940.4080.451818.5
    Rabbit2.3821.9590.5379.6217031
    Ferret2.7062.1740.4637.1190041
    Cat2.7842.280.6128.4400065
    Macaque3.272.4130.76193.85340165
    Short-tailed opossum2.2612.5080.717810513.5
    Dunnart2.5762.5080.6120.33213.5
    Wallaby3.1412.5080.9492011529.3
    Quoll2.7592.5080.653.3865018
    Brush-tailed opossum2.7932.5080.8719.4315017.5
    Quokka3.032.5080.88413.9270027
    Sheep2.9092.5330.82216045000147
    Human3.1673.720.654135070000270
    • Included data are species constant, precocial score, adult brain and body weight, and gestational length for each species.

    • View popup
    Table 3.

    List of location and process classifications with brief descriptions of each. All locations are determined by the starting area of the phenomenon that is observed

    Description
    Location
        Brain stemEncompasses the spinal cord, medulla, and mesencephalon
        CerebellumThe presumptive cerebellum
        Limbic systemAmygdala, hippocampus, septum, olfactory bulbs, olfactory, subicular, and entorhinal cortex
        ThalamusAll thalamic nuclei
        StriatumGlobus pallidus, caudate nucleus
        CortexIsocortex
        Whole brainGross brain growth
        Whole organismBehavioral events
        Sensory peripheryPeripheral nervous system
        RetinaRetina, retinal ganglion cells
    ProcessDescription
        NeurogenesisCell cycle exit for any group of cells
        Axon extensionWhen axons arrive at targets, form synapses, axon growth
        SegregationDifferentiation of a population of cells
        GABA cortexGABAergic cells that have origins in the striatum or isocortex
        Subtractive eventCell death
        Retinal wavesPatterns of developing retinal activity
        Synapse EliminationDecrease in synapse numbers
        SensorimotorBehavioral or reflexive event
        Brain growthGross brain development
        MyelinationFirst wrap of a glial cell around a neuron
        ElectrophysiologyOnset of electrical activity
    • View popup
    Table 4.

    Table of average SEPRED values by process and species

    ProcessRatMouseHumanGerbilShort-tailed opossumDunnartMacaqueWallabyQuollBrush-tailed opossumQuokkaHamsterSpiny mouseGuinea pigRabbitSheepFerretCat
    Neurogenesis0.060.070.140.110.100.110.090.090.100.090.100.060.040.100.080.100.080.08
    Axon extension0.050.060.110.090.090.090.070.080.080.080.080.050.040.080.060.080.070.07
    Segregation0.050.060.110.080.090.090.070.080.080.080.080.050.060.060.060.080.070.07
    GABA cortex0.060.070.140.110.100.110.090.100.100.100.100.060.030.090.080.100.080.08
    Subtractive event0.050.060.110.080.080.090.070.080.080.080.080.050.050.070.060.080.070.07
    Retinal waves0.060.060.120.080.090.100.080.090.090.090.090.060.070.060.070.090.080.08
    Synapse Elimination0.050.060.110.070.100.100.080.090.100.090.100.070.100.070.070.090.080.07
    Sensorimotor0.060.060.120.070.100.100.080.090.100.090.100.070.100.060.080.090.080.08
    Brain growth0.040.050.090.060.080.090.060.080.080.080.080.060.110.050.070.070.070.06
    Myelination0.050.060.100.060.090.100.070.090.090.090.090.060.100.060.070.080.070.07
    Electrophysiology0.050.060.110.060.090.100.070.090.090.090.090.060.090.060.070.080.070.07
Back to top

In this issue

The Journal of Neuroscience: 33 (17)
Journal of Neuroscience
Vol. 33, Issue 17
24 Apr 2013
  • Table of Contents
  • Table of Contents (PDF)
  • About the Cover
  • Index by author
  • Advertising (PDF)
  • Ed Board (PDF)
Email

Thank you for sharing this Journal of Neuroscience article.

NOTE: We request your email address only to inform the recipient that it was you who recommended this article, and that it is not junk mail. We do not retain these email addresses.

Enter multiple addresses on separate lines or separate them with commas.
Modeling Transformations of Neurodevelopmental Sequences across Mammalian Species
(Your Name) has forwarded a page to you from Journal of Neuroscience
(Your Name) thought you would be interested in this article in Journal of Neuroscience.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Print
View Full Page PDF
Citation Tools
Modeling Transformations of Neurodevelopmental Sequences across Mammalian Species
Alan D. Workman, Christine J. Charvet, Barbara Clancy, Richard B. Darlington, Barbara L. Finlay
Journal of Neuroscience 24 April 2013, 33 (17) 7368-7383; DOI: 10.1523/JNEUROSCI.5746-12.2013

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Respond to this article
Request Permissions
Share
Modeling Transformations of Neurodevelopmental Sequences across Mammalian Species
Alan D. Workman, Christine J. Charvet, Barbara Clancy, Richard B. Darlington, Barbara L. Finlay
Journal of Neuroscience 24 April 2013, 33 (17) 7368-7383; DOI: 10.1523/JNEUROSCI.5746-12.2013
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
  • Tweet Widget
  • Facebook Like
  • Google Plus One

Jump to section

  • Article
    • Abstract
    • Introduction
    • Materials and Methods
    • Results
    • Discussion
    • Footnotes
    • References
  • Figures & Data
  • Info & Metrics
  • eLetters
  • PDF

Responses to this article

Respond to this article

Jump to comment:

No eLetters have been published for this article.

Related Articles

Cited By...

More in this TOC Section

Articles

  • Choice Behavior Guided by Learned, But Not Innate, Taste Aversion Recruits the Orbitofrontal Cortex
  • Maturation of Spontaneous Firing Properties after Hearing Onset in Rat Auditory Nerve Fibers: Spontaneous Rates, Refractoriness, and Interfiber Correlations
  • Insulin Treatment Prevents Neuroinflammation and Neuronal Injury with Restored Neurobehavioral Function in Models of HIV/AIDS Neurodegeneration
Show more Articles

Development/Plasticity/Repair

  • Choice Behavior Guided by Learned, But Not Innate, Taste Aversion Recruits the Orbitofrontal Cortex
  • Maturation of Spontaneous Firing Properties after Hearing Onset in Rat Auditory Nerve Fibers: Spontaneous Rates, Refractoriness, and Interfiber Correlations
  • Insulin Treatment Prevents Neuroinflammation and Neuronal Injury with Restored Neurobehavioral Function in Models of HIV/AIDS Neurodegeneration
Show more Development/Plasticity/Repair
  • Home
  • Alerts
  • Visit Society for Neuroscience on Facebook
  • Follow Society for Neuroscience on Twitter
  • Follow Society for Neuroscience on LinkedIn
  • Visit Society for Neuroscience on Youtube
  • Follow our RSS feeds

Content

  • Early Release
  • Current Issue
  • Issue Archive
  • Collections

Information

  • For Authors
  • For Advertisers
  • For the Media
  • For Subscribers

About

  • About the Journal
  • Editorial Board
  • Privacy Policy
  • Contact
(JNeurosci logo)
(SfN logo)

Copyright © 2022 by the Society for Neuroscience.
JNeurosci Online ISSN: 1529-2401

The ideas and opinions expressed in JNeurosci do not necessarily reflect those of SfN or the JNeurosci Editorial Board. Publication of an advertisement or other product mention in JNeurosci should not be construed as an endorsement of the manufacturer’s claims. SfN does not assume any responsibility for any injury and/or damage to persons or property arising from or related to any use of any material contained in JNeurosci.